Mechanism of cold atmospheric plasma in treatment of chronic skin ulcer_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

YUAN Nanbing ¹ , YANG Yanzhi ¹ , TAN Cuixia ¹ ,  RAN Xingwu ²

1. Department of Endocrinology and Metabolism, the First People’s Hospital of Chengdu, Chengdu Sichuan, 610016, P. R. China;
2. Diabetic Foot Care Center, Department of Endocrinology and Metabolism, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P. R. China;

Corresponding author：

RAN Xingwu, Email: ranxingwu@163.com

Keywords：

Cold atmospheric plasma; chronic skin ulcer; disinfection; tissue regeneration

DOI：

10.7507/1002-1892.202404027

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the mechanism of cold atmospheric plasma (CAP) in the treatment of chronic skin ulcer, providing a new idea for ulcer therapy. Methods The literature about CAP in the treatment of chronic skin ulcers in recent years was extensively screened and reviewed. The treatment principle, active ingredients, and mechanism were summarized. Results CAP is partial ionized gas discharged by plasma generator in high frequency under high voltage. It contains electrons, positive and negative ions, reactive oxygen species, reactive nitrogen species, and ultraviolet rays. In vitro and animal experiments show that the active ingredients contained in CAP can inactive microorganisms, against biofilm, regulate immune-mediated inflammatory, promoting blood flow, stimulate tissue regeneration and epithelial formation in the course of wounds healing. Conclusion CAP play a role in different stages of chronic skin ulcer healing, with good efficacy and safety, and broad clinical application prospects. But more studies are needed to explore the indications and dosages of CAP therapy.

1.	Tabares FL, Junkar I. Cold plasma systems and their application in surface treatments for medicine. Molecules, 2021, 26(7): 1903. doi: 10.3390/molecules26071903.
2.	Liu P, Wang G, Ruan Q, et al. Plasma-activated interfaces for biomedical engineering. Bioact Mater, 2021, 6(7): 2134-2143.
3.	Setsuhara Y. Low-temperature atmospheric-pressure plasma sources for plasma medicine. Arch Biochem Biophys, 2016, 605(9): 3-10.
4.	Izadjoo M, Zack S, Kim H, et al. Medical applications of cold atmospheric plasma: state of the science. J Wound Care, 2018, 27(Sup9): S4-S10.
5.	Karthik C, Sarngadharan SC, Thomas V. Low-temperature plasma techniques in biomedical applications and therapeutics: an overview. Int J Mol Sci, 2023, 25(1): 524. doi: 10.3390/ijms25010524.
6.	Lin SP, Khumsupan D, Chou YJ, et al. Applications of atmospheric cold plasma in agricultural, medical, and bioprocessing industries. Appl Microbiol Biotechnol, 2022, 106(23): 7737-7750.
7.	Lunder M, Dahle S, Fink R. Cold atmospheric plasma for surface disinfection: a promising weapon against deleterious meticillin-resistant Staphylococcus aureus biofilms. J Hosp Infect, 2024, 143(1): 64-75.
8.	Khumsupan D, Lin SP, Hsieh CW, et al. Current and potential applications of atmospheric cold plasma in the food industry. Molecules, 2023, 28(13): 4903. doi: 10.3390/molecules28134903.
9.	Dai X, Wu J, Lu L, et al. Current status and future trends of cold atmospheric plasma as an oncotherapy. Biomol Ther, 2023, 31(5): 496-514.
10.	Canady J, Murthy SR, Zhuang T, et al. The first cold atmospheric plasma phase Ⅰ clinical trial for the treatment of advanced solid tumors: a novel treatment arm for cancer. Cancers, 2023, 15(14): 3688. doi: 10.3390/cancers15143688.
11.	Alqutaibi AY, Aljohani A, Alduri A, et al. The effectiveness of cold atmospheric plasma (CAP) on bacterial reduction in dental implants: a systematic review. Biomolecules, 2023, 13(10): 1528. doi: 10.3390/biom13101528.
12.	Bai F, Ran Y, Zhai S, et al. Cold atmospheric plasma: a promising and safe therapeutic strategy for atopic dermatitis. Int Arch Allergy Immunol, 2023, 184(12): 1184-1197.
13.	Sen CK. Human wound and its burden: updated 2022 compendium of estimates. Adv Wound Care, 2023, 12(12): 657-670.
14.	Nguyen TX, Nguyen DH, Ho-Man TP, et al. Cold plasmamed beam as a supporting treatment of soft tissue injuries in severe covid-19 patients: a preliminary report. Med Devices, 2022, 15(8): 277-283.
15.	Samsavar S, Mahmoudi H, Khani MR, et al. Treatment of chronic venous ulcer with cold atmospheric plasma jet. Case Rep Dermatol, 2022, 14(3): 344-349.
16.	Strohal R, Dietrich S, Mittlbock M, et al. Chronic wounds treated with cold atmospheric plasmajet versus best practice wound dressings: a multicenter, randomized, non-inferiority trial. Sci Rep, 2022, 12(1): 3645. doi: 10.1038/s41598-022-07333-x.
17.	Bernhardt T, Semmler ML, Schäfer M, et al. Plasma medicine: applications of cold atmospheric pressure plasma in dermatology. Oxid Med Cell Longev, 2019, 2019: 3873928. doi: 10.1155/2019/3873928.
18.	Gan L, Jiang J, Duan JW, et al. Cold atmospheric plasma applications in dermatology: A systematic review. J Biophotonics, 2021, 14(3): e202000415. doi: 10.1002/jbio.202000415.
19.	von Woedtke T, Emmert S, Metelmann HR, et al. Perspectives on cold atmospheric plasma (CAP) applications in medicine. Phys Plasmas, 2020, 27: 070601. doi: 10.1063/5.0008093.
20.	Hong Q, Dong X, Jones JE, et al. A novel approach to expedite wound healing with plasma brush of cold flame. Rev Sci Instrum, 2023, 94(8): 084102. doi: 10.1063/5.0096969.
21.	Feibel D, Golda J, Held J, et al. Gas flow-dependent modification of plasma chemistry in μAPP jet-generated cold atmospheric plasma and its impact on human skin fibroblasts. Biomedicines, 2023, 11(5): 1242. doi: 10.3390/biomedicines11051242.
22.	Bakhtiyari-Ramezani M, Nohekhan M, Akbari ME, et al. Comparative assessment of direct and indirect cold atmospheric plasma effects, based on helium and argon, on human glioblastoma: an in vitro and in vivo study. Sci Rep, 2024, 14(1): 3578. doi: 10.1038/s41598-024-54070-4.
23.	Tan F, Wang Y, Zhang S, et al. Plasma dermatology: skin therapy using cold atmospheric plasma. Front Oncol, 2022, 12: 918484. doi: 10.3389/fonc.2022.918484.
24.	Hofmann AG, Deinsberger J, Oszwald A, et al. The histopathology of leg ulcers. Dermatopathology, 2024, 11(1): 62-78.
25.	Wilkinson HN, Hardman MJ. Wound healing: cellular mechanisms and pathological outcomes. Open Biol, 2020, 10(9): 200223. doi: 10.1098/rsob.200223.
26.	Carr MA, Marquart ME, Sanchez M, et al. Innovative cold atmospheric plasma (iCAP) decreases corneal ulcer formation and bacterial loads and improves anterior chamber health in methicillin resistant Staphylococcus aureus keratitis. Exp Eye Res, 2023, 237: 109692. doi: 10.1016/j.exer.2023.109692.
27.	Kremer J, Meinert EFRC, Farag M, et al. New wound management of driveline infections with cold atmospheric plasma. J Cardiovasc Dev Dis, 2022, 9(11): 405. doi: 10.3390/jcdd9110405.
28.	Kaushik N, Mitra S, Baek EJ, et al. The inactivation and destruction of viruses by reactive oxygen species generated through physical and cold atmospheric plasma techniques: Current status and perspectives. J Adv Res, 2023, 43: 59-71.
29.	Fink S, Fischer M, Spange S, et al. Cold atmospheric plasma exerts antimicrobial effects in a 3D skin model of cutaneous candidiasis. Antibiotics, 2023, 12(5): 933. doi: 10.3390/antibiotics12050933.
30.	Nam G, Kim M, Jang Y, et al. Cold atmospheric pressure microplasma pipette for disinfection of methicillin-resistant staphylococcus aureus. Micromachines, 2021, 12(9): 1103. doi: 10.3390/mi12091103.
31.	Mohd Nasir N, Lee BK, Yap SS, et al. Cold plasma inactivation of chronic wound bacteria. Arch Biochem Biophys, 2016, 605: 76-85.
32.	Zhang H, Zhang C, Han Q. Mechanisms of bacterial inhibition and tolerance around cold atmospheric plasma. Appl Microbiol Biotechnol, 2023, 107(17): 5301-5316.
33.	Wang J, Yu Z, Xu Z, et al. Antimicrobial mechanism and the effect of atmospheric pressure N2 plasma jet on the regeneration capacity of Staphylococcus aureus biofilm. Biofouling, 2018, 34(8): 935-949.
34.	Guo L, Yang L, Qi Y, et al. Low-temperature gas plasma combined with antibiotics for the reduction of methicillin-resistant staphylococcus aureus biofilm both in vitro and in vivo. Life (Basel), 2021, 11(8): 828. doi: 10.3390/life11080828.
35.	Maybin JA, Thompson TP, Flynn PB, et al. Cold atmospheric pressure plasma-antibiotic synergy in pseudomonas aeruginosa biofilms is mediated via oxidative stress response. Biofilm, 2023, 5: 100122. doi: 10.1016/j.bioflm.2023.100122.
36.	Baz A, Bakri A, Butcher M et al. Staphylococcus aureus strains exhibit heterogenous tolerance to direct cold atmospheric plasma therapy. Biofilm, 2023, 5: 100123. doi: 10.1016/j.bioflm.2023.100123.
37.	Bagheri M, von Kohout M, Zoric A, et al. Can cold atmospheric plasma be used for infection control in burns? A preclinical evaluation. Biomedicines, 2023, 11(5): 1239. doi: 10.3390/biomedicines11051239.
38.	Li Y, Nie L, Jin S, et al. The effect of plasma on bacteria and normal cells in infected wound. Oxid Med Cell Longev, 2022, 2022: 1838202. doi: 10.1155/2022/1838202.
39.	Mirpour S, Fathollah S, Mansouri P, et al. Cold atmospheric plasma as an effective method to treat diabetic foot ulcers: A randomized clinical trial. Sci Rep, 2020, 10(1): 10440. doi: 10.1038/s41598-020-67232-x.
40.	Ma Y, Sun T, Ren K, Min T, et al. Applications of cold atmospheric plasma in immune-mediated inflammatory diseases via redox homeostasis: evidence and prospects. Heliyon, 2023, 9(12): e22568. doi: 10.1016/j.heliyon.2023.e22568.
41.	Kupke LS, Arndt S, Lenzer S, et al. Cold atmospheric plasma promotes the immunoreactivity of granulocytes in vitro. Biomolecules, 2021, 11(6): 902. doi: 10.3390/biom11060902.
42.	Hämmerle G, Ascher S, Gebhardt L. Positive effects of cold atmospheric plasma on pH in wounds: a pilot study. J Wound Care, 2023, 32(9): 530-536.
43.	Arndt S, Unger P, Berneburg M, et al. Cold atmospheric plasma (CAP) activates angiogenesis-related molecules in skin keratinocytes, fibroblasts and endothelial cells and improves wound angiogenesis in an autocrine and paracrine mode. J Dermatol Sci, 2018, 89(2): 181-190.
44.	Arndt S, Unger P, Wacker E, et al. Cold atmospheric plasma (CAP) changes gene expression of key molecules of the wound healing machinery and improves wound healing in vitro and in vivo. PLoS One, 2013, 8(11): e79325. doi: 10.1371/journal.pone.0079325.
45.	Borchardt T, Helmke A, Ernst J, et al. Topically confined enhancement of cutaneous microcirculation by cold plasma. Skin Pharmacol Physiol, 2022, 35(6): 343-353.
46.	Shekhter AB, Pekshev AV, Vagapov AB, et al. Physicochemical parameters of NO-containing gas flow affect wound healing therapy. An experimental study. Eur J Pharm Sci, 2019, 128: 193-201.
47.	Schmidt A, Liebelt G, Niebner F, et al. Gas plasma-spurred wound healing is accompanied by regulation of focal adhesion, matrix remodeling, and tissue oxygenation. Redox Biol, 2021, 38: 101809. doi: 10.1016/j.redox.2020.101809.
48.	Rognoni E, Walko G. The roles of YAP/TAZ and the Hippo pathway in healthy and diseased skin. Cells, 2019, 8(5): 411. doi: 10.3390/cells8050411.
49.	Shome D, Woedtke T, Riedel K, et al. The HIPPO transducer YAP and its targets CTGF and Cyr61 drive a paracrine signalling in cold atmospheric plasma-mediated wound healing. Oxid Med Cell Longev, 2020, 2020: 4910280. doi: 10.1155/2020/4910280.
50.	Bekeschus S, Kramer A, Schmidt A. Gas plasma-augmented wound healing in animal models and veterinary medicine. Molecules, 2021, 26(18): 5682. doi: 10.3390/molecules26185682.
51.	Ma L, Chen Y, Gong Q, et al. Cold atmospheric plasma alleviates radiation-induced skin injury by suppressing inflammation and promoting repair. Free Radic Biol Med, 2023, 204: 184-194.
52.	He R, Shen W, Wang T, et al. The efficacy and safety of cold atmospheric plasma as a novel therapy for diabetic wound in vitro and in vivo. Int Wound J, 2020, 17(3): 851-863.
53.	Tatlıcıoğlu G, Çürükoğlu A, Akan G, et al. Effect of cold atmospheric plasma/NO gas application with different exposure times on healing in wounds with tissue loss in diabetic rats. Pol J Vet Sci, 2023, 26(3): 441-447.
54.	Badr G, EI-Hossary FM, Lasheen FEM, et al. Cold atmospheric plasma induces the curing mechanism of diabetic wounds by regulating the oxidative stress mediators iNOS and NO, the pyroptotic mediators NLRP-3, Caspase-1 and IL-1β and the angiogenesis mediators VEGF and Ang-1. Biomed Pharmacother, 2023, 169: 115934. doi: 10.1016/j.biopha.2023.115934.
55.	Yoo J, Kang Y, Baek SJ, et al. Application of cold atmospheric microwave plasma as an adjunct therapy for wound healing in dogs and cats. J Vet Sci, 2023, 24(4): e56. doi: 10.4142/jvs.23067.
56.	Rutkowski R, Daeschlein G, Woedtke T, et al. Long-term risk assessment for medical application of cold atmospheric pressure plasma. Diagnostics, 2020, 10(4): 210. doi: 10.3390/diagnostics10040210.
57.	Ermakov A, Ermakova, Afanasyva, et al. Dose-dependent effects of cold atmospheric argon plasma on the mesenchymal stem and osteosarcoma cells in vitro. Int J Mol Sci, 2021, 22(13): 6797. doi: 10.3390/ijms22136797.
58.	Samsavar S, Mahmoudi H, Shakouri R, et al. The evaluation of efficacy of atmospheric pressure plasma in diabetic ulcers healing: A randomized clinical trial. Dermatol Ther, 2021, 34(6): e15169. doi: 10.1111/dth.15169.

1. Tabares FL, Junkar I. Cold plasma systems and their application in surface treatments for medicine. Molecules, 2021, 26(7): 1903. doi: 10.3390/molecules26071903.
2. Liu P, Wang G, Ruan Q, et al. Plasma-activated interfaces for biomedical engineering. Bioact Mater, 2021, 6(7): 2134-2143.
3. Setsuhara Y. Low-temperature atmospheric-pressure plasma sources for plasma medicine. Arch Biochem Biophys, 2016, 605(9): 3-10.
4. Izadjoo M, Zack S, Kim H, et al. Medical applications of cold atmospheric plasma: state of the science. J Wound Care, 2018, 27(Sup9): S4-S10.
5. Karthik C, Sarngadharan SC, Thomas V. Low-temperature plasma techniques in biomedical applications and therapeutics: an overview. Int J Mol Sci, 2023, 25(1): 524. doi: 10.3390/ijms25010524.
6. Lin SP, Khumsupan D, Chou YJ, et al. Applications of atmospheric cold plasma in agricultural, medical, and bioprocessing industries. Appl Microbiol Biotechnol, 2022, 106(23): 7737-7750.
7. Lunder M, Dahle S, Fink R. Cold atmospheric plasma for surface disinfection: a promising weapon against deleterious meticillin-resistant Staphylococcus aureus biofilms. J Hosp Infect, 2024, 143(1): 64-75.
8. Khumsupan D, Lin SP, Hsieh CW, et al. Current and potential applications of atmospheric cold plasma in the food industry. Molecules, 2023, 28(13): 4903. doi: 10.3390/molecules28134903.
9. Dai X, Wu J, Lu L, et al. Current status and future trends of cold atmospheric plasma as an oncotherapy. Biomol Ther, 2023, 31(5): 496-514.
10. Canady J, Murthy SR, Zhuang T, et al. The first cold atmospheric plasma phase Ⅰ clinical trial for the treatment of advanced solid tumors: a novel treatment arm for cancer. Cancers, 2023, 15(14): 3688. doi: 10.3390/cancers15143688.
11. Alqutaibi AY, Aljohani A, Alduri A, et al. The effectiveness of cold atmospheric plasma (CAP) on bacterial reduction in dental implants: a systematic review. Biomolecules, 2023, 13(10): 1528. doi: 10.3390/biom13101528.
12. Bai F, Ran Y, Zhai S, et al. Cold atmospheric plasma: a promising and safe therapeutic strategy for atopic dermatitis. Int Arch Allergy Immunol, 2023, 184(12): 1184-1197.
13. Sen CK. Human wound and its burden: updated 2022 compendium of estimates. Adv Wound Care, 2023, 12(12): 657-670.
14. Nguyen TX, Nguyen DH, Ho-Man TP, et al. Cold plasmamed beam as a supporting treatment of soft tissue injuries in severe covid-19 patients: a preliminary report. Med Devices, 2022, 15(8): 277-283.
15. Samsavar S, Mahmoudi H, Khani MR, et al. Treatment of chronic venous ulcer with cold atmospheric plasma jet. Case Rep Dermatol, 2022, 14(3): 344-349.
16. Strohal R, Dietrich S, Mittlbock M, et al. Chronic wounds treated with cold atmospheric plasmajet versus best practice wound dressings: a multicenter, randomized, non-inferiority trial. Sci Rep, 2022, 12(1): 3645. doi: 10.1038/s41598-022-07333-x.
17. Bernhardt T, Semmler ML, Schäfer M, et al. Plasma medicine: applications of cold atmospheric pressure plasma in dermatology. Oxid Med Cell Longev, 2019, 2019: 3873928. doi: 10.1155/2019/3873928.
18. Gan L, Jiang J, Duan JW, et al. Cold atmospheric plasma applications in dermatology: A systematic review. J Biophotonics, 2021, 14(3): e202000415. doi: 10.1002/jbio.202000415.
19. von Woedtke T, Emmert S, Metelmann HR, et al. Perspectives on cold atmospheric plasma (CAP) applications in medicine. Phys Plasmas, 2020, 27: 070601. doi: 10.1063/5.0008093.
20. Hong Q, Dong X, Jones JE, et al. A novel approach to expedite wound healing with plasma brush of cold flame. Rev Sci Instrum, 2023, 94(8): 084102. doi: 10.1063/5.0096969.
21. Feibel D, Golda J, Held J, et al. Gas flow-dependent modification of plasma chemistry in μAPP jet-generated cold atmospheric plasma and its impact on human skin fibroblasts. Biomedicines, 2023, 11(5): 1242. doi: 10.3390/biomedicines11051242.
22. Bakhtiyari-Ramezani M, Nohekhan M, Akbari ME, et al. Comparative assessment of direct and indirect cold atmospheric plasma effects, based on helium and argon, on human glioblastoma: an in vitro and in vivo study. Sci Rep, 2024, 14(1): 3578. doi: 10.1038/s41598-024-54070-4.
23. Tan F, Wang Y, Zhang S, et al. Plasma dermatology: skin therapy using cold atmospheric plasma. Front Oncol, 2022, 12: 918484. doi: 10.3389/fonc.2022.918484.
24. Hofmann AG, Deinsberger J, Oszwald A, et al. The histopathology of leg ulcers. Dermatopathology, 2024, 11(1): 62-78.
25. Wilkinson HN, Hardman MJ. Wound healing: cellular mechanisms and pathological outcomes. Open Biol, 2020, 10(9): 200223. doi: 10.1098/rsob.200223.
26. Carr MA, Marquart ME, Sanchez M, et al. Innovative cold atmospheric plasma (iCAP) decreases corneal ulcer formation and bacterial loads and improves anterior chamber health in methicillin resistant Staphylococcus aureus keratitis. Exp Eye Res, 2023, 237: 109692. doi: 10.1016/j.exer.2023.109692.
27. Kremer J, Meinert EFRC, Farag M, et al. New wound management of driveline infections with cold atmospheric plasma. J Cardiovasc Dev Dis, 2022, 9(11): 405. doi: 10.3390/jcdd9110405.
28. Kaushik N, Mitra S, Baek EJ, et al. The inactivation and destruction of viruses by reactive oxygen species generated through physical and cold atmospheric plasma techniques: Current status and perspectives. J Adv Res, 2023, 43: 59-71.
29. Fink S, Fischer M, Spange S, et al. Cold atmospheric plasma exerts antimicrobial effects in a 3D skin model of cutaneous candidiasis. Antibiotics, 2023, 12(5): 933. doi: 10.3390/antibiotics12050933.
30. Nam G, Kim M, Jang Y, et al. Cold atmospheric pressure microplasma pipette for disinfection of methicillin-resistant staphylococcus aureus. Micromachines, 2021, 12(9): 1103. doi: 10.3390/mi12091103.
31. Mohd Nasir N, Lee BK, Yap SS, et al. Cold plasma inactivation of chronic wound bacteria. Arch Biochem Biophys, 2016, 605: 76-85.
32. Zhang H, Zhang C, Han Q. Mechanisms of bacterial inhibition and tolerance around cold atmospheric plasma. Appl Microbiol Biotechnol, 2023, 107(17): 5301-5316.
33. Wang J, Yu Z, Xu Z, et al. Antimicrobial mechanism and the effect of atmospheric pressure N2 plasma jet on the regeneration capacity of Staphylococcus aureus biofilm. Biofouling, 2018, 34(8): 935-949.
34. Guo L, Yang L, Qi Y, et al. Low-temperature gas plasma combined with antibiotics for the reduction of methicillin-resistant staphylococcus aureus biofilm both in vitro and in vivo. Life (Basel), 2021, 11(8): 828. doi: 10.3390/life11080828.
35. Maybin JA, Thompson TP, Flynn PB, et al. Cold atmospheric pressure plasma-antibiotic synergy in pseudomonas aeruginosa biofilms is mediated via oxidative stress response. Biofilm, 2023, 5: 100122. doi: 10.1016/j.bioflm.2023.100122.
36. Baz A, Bakri A, Butcher M et al. Staphylococcus aureus strains exhibit heterogenous tolerance to direct cold atmospheric plasma therapy. Biofilm, 2023, 5: 100123. doi: 10.1016/j.bioflm.2023.100123.
37. Bagheri M, von Kohout M, Zoric A, et al. Can cold atmospheric plasma be used for infection control in burns? A preclinical evaluation. Biomedicines, 2023, 11(5): 1239. doi: 10.3390/biomedicines11051239.
38. Li Y, Nie L, Jin S, et al. The effect of plasma on bacteria and normal cells in infected wound. Oxid Med Cell Longev, 2022, 2022: 1838202. doi: 10.1155/2022/1838202.
39. Mirpour S, Fathollah S, Mansouri P, et al. Cold atmospheric plasma as an effective method to treat diabetic foot ulcers: A randomized clinical trial. Sci Rep, 2020, 10(1): 10440. doi: 10.1038/s41598-020-67232-x.
40. Ma Y, Sun T, Ren K, Min T, et al. Applications of cold atmospheric plasma in immune-mediated inflammatory diseases via redox homeostasis: evidence and prospects. Heliyon, 2023, 9(12): e22568. doi: 10.1016/j.heliyon.2023.e22568.
41. Kupke LS, Arndt S, Lenzer S, et al. Cold atmospheric plasma promotes the immunoreactivity of granulocytes in vitro. Biomolecules, 2021, 11(6): 902. doi: 10.3390/biom11060902.
42. Hämmerle G, Ascher S, Gebhardt L. Positive effects of cold atmospheric plasma on pH in wounds: a pilot study. J Wound Care, 2023, 32(9): 530-536.
43. Arndt S, Unger P, Berneburg M, et al. Cold atmospheric plasma (CAP) activates angiogenesis-related molecules in skin keratinocytes, fibroblasts and endothelial cells and improves wound angiogenesis in an autocrine and paracrine mode. J Dermatol Sci, 2018, 89(2): 181-190.
44. Arndt S, Unger P, Wacker E, et al. Cold atmospheric plasma (CAP) changes gene expression of key molecules of the wound healing machinery and improves wound healing in vitro and in vivo. PLoS One, 2013, 8(11): e79325. doi: 10.1371/journal.pone.0079325.
45. Borchardt T, Helmke A, Ernst J, et al. Topically confined enhancement of cutaneous microcirculation by cold plasma. Skin Pharmacol Physiol, 2022, 35(6): 343-353.
46. Shekhter AB, Pekshev AV, Vagapov AB, et al. Physicochemical parameters of NO-containing gas flow affect wound healing therapy. An experimental study. Eur J Pharm Sci, 2019, 128: 193-201.
47. Schmidt A, Liebelt G, Niebner F, et al. Gas plasma-spurred wound healing is accompanied by regulation of focal adhesion, matrix remodeling, and tissue oxygenation. Redox Biol, 2021, 38: 101809. doi: 10.1016/j.redox.2020.101809.
48. Rognoni E, Walko G. The roles of YAP/TAZ and the Hippo pathway in healthy and diseased skin. Cells, 2019, 8(5): 411. doi: 10.3390/cells8050411.
49. Shome D, Woedtke T, Riedel K, et al. The HIPPO transducer YAP and its targets CTGF and Cyr61 drive a paracrine signalling in cold atmospheric plasma-mediated wound healing. Oxid Med Cell Longev, 2020, 2020: 4910280. doi: 10.1155/2020/4910280.
50. Bekeschus S, Kramer A, Schmidt A. Gas plasma-augmented wound healing in animal models and veterinary medicine. Molecules, 2021, 26(18): 5682. doi: 10.3390/molecules26185682.
51. Ma L, Chen Y, Gong Q, et al. Cold atmospheric plasma alleviates radiation-induced skin injury by suppressing inflammation and promoting repair. Free Radic Biol Med, 2023, 204: 184-194.
52. He R, Shen W, Wang T, et al. The efficacy and safety of cold atmospheric plasma as a novel therapy for diabetic wound in vitro and in vivo. Int Wound J, 2020, 17(3): 851-863.
53. Tatlıcıoğlu G, Çürükoğlu A, Akan G, et al. Effect of cold atmospheric plasma/NO gas application with different exposure times on healing in wounds with tissue loss in diabetic rats. Pol J Vet Sci, 2023, 26(3): 441-447.
54. Badr G, EI-Hossary FM, Lasheen FEM, et al. Cold atmospheric plasma induces the curing mechanism of diabetic wounds by regulating the oxidative stress mediators iNOS and NO, the pyroptotic mediators NLRP-3, Caspase-1 and IL-1β and the angiogenesis mediators VEGF and Ang-1. Biomed Pharmacother, 2023, 169: 115934. doi: 10.1016/j.biopha.2023.115934.
55. Yoo J, Kang Y, Baek SJ, et al. Application of cold atmospheric microwave plasma as an adjunct therapy for wound healing in dogs and cats. J Vet Sci, 2023, 24(4): e56. doi: 10.4142/jvs.23067.
56. Rutkowski R, Daeschlein G, Woedtke T, et al. Long-term risk assessment for medical application of cold atmospheric pressure plasma. Diagnostics, 2020, 10(4): 210. doi: 10.3390/diagnostics10040210.
57. Ermakov A, Ermakova, Afanasyva, et al. Dose-dependent effects of cold atmospheric argon plasma on the mesenchymal stem and osteosarcoma cells in vitro. Int J Mol Sci, 2021, 22(13): 6797. doi: 10.3390/ijms22136797.
58. Samsavar S, Mahmoudi H, Shakouri R, et al. The evaluation of efficacy of atmospheric pressure plasma in diabetic ulcers healing: A randomized clinical trial. Dermatol Ther, 2021, 34(6): e15169. doi: 10.1111/dth.15169.

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